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01-01-2005 | Research Article

Inhibitory effect of capsaicin evoked trigeminal pain on warmth sensation and warmth evoked potentials

Authors: Massimiliano Valeriani, Michele Tinazzi, Domenica Le Pera, Domenico Restuccia, Liala De Armas, Toni Maiese, Pietro Tonali, Lars Arendt-Nielsen

Published in: Experimental Brain Research | Issue 1/2005

Abstract

The aim of the study was to evaluate the effect of tonic pain evoked by topical application of capsaicin on the somatosensory sensation of warmth. The warmth pathways were studied in ten healthy subjects by recording the scalp potentials evoked by non-painful warm laser stimuli delivered on both the right and left perioral region (warmth C-fiber related laser-evoked potentials (C-LEPs)). Tonic pain was induced by topical capsaicin application above the lateral part of the right upper lip. The area of primary and secondary hyperalgesia were mapped. C-LEPs were obtained from 31 scalp electrodes before, during, and after capsaicin application. C-LEPs from the right perioral region were evoked by laser stimuli delivered to the area of secondary hyperalgesia during capsaicin application and on both the areas of primary and secondary hyperalgesia after capsaicin removal. While the lateralized N1/P1 component (around 185 ms of latency) was not affected by the capsaicin, the amplitudes of the later vertex C-LEPs (around 260 and 410 ms of latency for the N2a and P2 potentials, respectively) evoked from the secondary hyperalgesic area on the right side and from a symmetrical non-hyperalgesic area on the left perioral region were significantly decreased during capsaicin application and after capsaicin removal, as compared with the baseline recordings. At the same times, the rating of the laser-evoked warmth sensation was reduced significantly. This inhibitory effect can occur at brainstem level and is possibly due to: 1) trigemino-cortico-trigeminal circuits, similar to those mediating the classical diffuse noxious inhibitory control, or 2) an increased background activity of the capsaicin-insensitive A-fibers, which mediate the secondary hyperalgesia. Probably due to a peripheral inhibitory mechanism, neither reliable C-LEP components nor warmth sensation were evoked by laser pulses delivered to the primary hyperalgesic area. This is the first neurophysiological evidence in humans of an inhibitory effect of pain on warmth sensation.

Agostino R, Cruccu G, Iannetti G, Romaniello A, Truini A, Manfredi M (2000) Topographical distribution of pinprick and warmth thresholds to CO2 laser stimulation on the human skin. Neurosci Lett 285:115–118CrossRefPubMed

Ali Z, Meyer RA, Campbell JN (1996) Secondary hyperalgesia to mechanical but not heat stimuli following a capsaicin injection in hairy skin. Pain 68:401–411CrossRefPubMed

Alper BS, Lewis PR (2002) Treatment of postherpetic neuralgia: a systematic review of the literature. J Fam Pract 51:121–128PubMed

Andersen OK, Jensen LM, Brennum J, Arendt-Nielsen L (1994) Evidence for central summation of C and A delta nociceptive activity in man. Pain 59:273–280CrossRefPubMed

Andrew D, Craig AD (2001) Spinothalamic lamina I neurones selectively responsive to cutaneous warming in cats. J Physiol 537:489–495PubMed

Arendt-Nielsen L, Gotliebsen K (1992) Segmental inhibition of laser-evoked brain potentials by ipsi- and contralaterally applied cold pressor pain. Eur J Appl Physiol Occup Physiol 64:56–61PubMed

Baumann TK, Simone DA, Shain CN, LaMotte RH (1991) Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J Neurophysiol 66:212–227PubMed

Beydoun A, Dyke DB, Morrow TJ, Casey KL (1996) Topical capsaicin selectively attenuates heat pain and A delta fiber-mediated laser-evoked potentials. Pain 65:189–196CrossRefPubMed

Bini G, Cruccu G, Hagbarth KE, Schady W, Torebjork E (1984) Analgesic effect of vibration and cooling on pain induced by intraneural electrical stimulation. Pain 18:239–248CrossRefPubMed

Bjerring P, Arendt-Nielsen L (1988) Argon laser induced single cortical responses: a new method to quantify pre-pain and pain perceptions. J Neurol Neurosurg Psichiatry 51:43–49

Bjerring P, Arendt-Nielsen L (1989) Use of a new argon laser technique to evaluate changes in sensory and pain thresholds in human skin following topical capsaicin treatment. Skin Pharmacol 2:162–167PubMed

Bragard D, Chen AC, Plaghki L (1996) Direct isolation of ultra-late (C-fibre) evoked brain potentials by CO2 laser stimulation of tiny cutaneous surface areas in man. Neurosci Lett 209:81–84

Bromm B, Lorenz J (1998) Neurophysiological evaluation of pain. Electroencephalogr Clin Neurophysiol 107:227–253CrossRefPubMed

Bromm B, Treede RD (1984) Nerve fibre discharges, cerebral potentials and sensations induced by CO2 laser stimulation. Hum Neurobiol 3:33–40PubMed

Bromm B, Treede RD (1991) Laser-evoked cerebral potentials in the assessment of cutaneous pain sensitivity in normal subjects and patients. Rev Neurol 147:625–643PubMed

Casey KL, Minoshima S, Morrow TJ, Koeppe RA (1996) Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. J Neurophysiol 76:571–581PubMed

Craig AD, Dostrovsky JO (2001) Differential projections of thermoreceptive and nociceptive lamina I trigeminothalamic and spinothalamic neurons in the cat. J Neurophysiol 86:856–870PubMed

Cruccu G, Pennisi E, Truini A, Iannetti GD, Romaniello A, Le Pera D, De Armas L, Leandri M, Manfredi M, Valeriani M (2003) Unmyelinated trigeminal pathways as assessed by laser stimuli in humans. Brain 126:2246–2256CrossRefPubMed

Darian-Smith I, Johnson KO, LaMotte C, Shigenaga Y, Kenins P, Champness P (1979) Warm fibers innervating palmar and digital skin of the monkey: responses to thermal stimuli. J Neurophysiol 42:1297–1315PubMed

Derbyshire SW, Jones AK, Gyulai F, Clark S, Townsend D, Firestone LL (1997) Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73:431–445CrossRefPubMed

Dickenson AH, Hellon RF, Taylor DC (1979) Facial thermal input to the trigeminal spinal nucleus of rabbits and rats. J Comp Neurol 185:203–209PubMed

Dougherty PM, Willis WD, Lenz FA (1998) Transient inhibition of responses to thermal stimuli of spinal sensory tract neurons in monkeys during sensitization by intradermal capsaicin. Pain 77:129–136CrossRefPubMed

Duclaux R, Kenshalo DR Sr (1980) Response characteristics of cutaneous warm receptors in the monkey. J Neurophysiol 43:1–15PubMed

Ellrich J, Treede RD (1998) Characterization of blink reflex interneurons by activation of diffuse noxious inhibitory controls in man. Brain Res 803:161–168CrossRefPubMed

Fitzgerald M (1983) Capsaicin and sensory neurones—a review. Pain 15:109–130CrossRefPubMed

Green BG, Cruz A (1998) “Warmth-insensitive fields”: evidence of sparse and irregular innervation of human skin by the warmth sense. Somatosens Mot Res 15:269–275CrossRefPubMed

Greenspan JD, Kenshalo DR Sr (1985) The primate as a model for the human temperature-sensing system: 2. Area of skin receiving thermal stimulation (spatial summation). Somatosens Res 2:315–324PubMed

Han ZS, Zhang ET, Craig AD (1998) Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nat Neurosci 1:218–225CrossRefPubMed

Hensel H, Iggo A (1971) Analysis of cutaneous warm and cold fibres in primates. Pflugers Arch 329:1–8PubMed

Iannetti GD, Truini A, Romaniello A, Galeotti F, Rizzo C, Manfredi M, Cruccu G (2003a) Evidence of a specific spinal pathway for the sense of warmth in humans. J Neurophysiol 89:562–570PubMed

Iannetti GD, Porro CA, Pantano P, Romanelli PL, Galeotti F, Cruccu G (2003b) Representation of different trigeminal divisions within the primary and secondary human somatosensory cortex. Neuroimage 19:906–912CrossRefPubMed

LaMotte RH, Campbell JN (1978) Comparison of responses of warm and nociceptive C-fiber afferents in monkey with human judgments of thermal pain. J Neurophysiol 41:509–528PubMed

Le Bars D, Dickenson AH, Besson JM (1979a) Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6:283–304CrossRefPubMed

Le Bars D, Dickenson AH, Besson JM (1979b) Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 6:305–327CrossRefPubMed

Liu XG, Morton CR, Azkue JJ, Zimmermann M, Sandkuhler J (1998) Long-term depression of C-fibre-evoked spinal field potentials by stimulation of primary afferent A delta-fibres in the adult rat. Eur J Neurosci 10:3069–3075CrossRefPubMed

Magerl W, Fuchs PN, Meyer RA, Treede R-D (2001) Roles of capsaicin-insensitive nociceptors in cutaneous pain and secondary hyperalgesia. Brain 9:1754–1764CrossRef

Manger PR, Woods TM, Jones EG (1996) Representation of face and intra-oral structures in area 3b of macaque monkey somatosensory cortex. J Comp Neurol 371:513–521CrossRefPubMed

Marks LE, Stevens JC (1973) Spatial summation of warmth: influence of duration and configuration of the stimulus. Am J Psychol 86:251–267PubMed

Mouraux A, Guerit JM, Plaghki L (2003) Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between A partial partial differential- and C-fibre afferent volleys. Clin Neurophysiol 114:710–722CrossRefPubMed

Perrin F, Pernier J, Bertrand O, Giard MH, Echallier JF (1987) Mapping of scalp potentials by surface spline interpolation. Electroencephalogr Clin Neurophysiol 66:75–81CrossRefPubMed

Plaghki L, Bragard D, Le Bars D, Willer JC, Godfraind JM (1998) Facilitation of a nociceptive flexion reflex in man by nonnoxious radiant heat produced by a laser. J Neurophysiol 79:2557–1567PubMed

Qiu Y, Inui K, Wang X, Tran TD, Kakigi R (2002) Effects of attention, distraction and sleep on CO(2) laser evoked potentials related to C-fibers in humans. Clin Neurophysiol 113:1579–1585CrossRefPubMed

Romaniello A, Arendt-Nielsen L, Cruccu G, Svensson P (2002) Modulation of trigeminal laser evoked potentials and laser silent periods by homotopical experimental pain. Pain 98:217–228CrossRefPubMed

Ross DR, Varipapa RJ (1989) Treatment of painful diabetic neuropathy with topical capsaicin. N Engl J Med 321:474–475

Serra J, Campero M, Ochoa J (1998) Flare and hyperalgesia after intradermal capsaicin injection in human skin. J Neurophysiol 80:2801–2810PubMed

Stevens JC, Marks LE, Simonson DC (1974) Regional sensitivity and spatial summation in the warmth sense. Physiol Behav 13:825–836CrossRefPubMed

Talbot JD, Duncan GH, Bushnell MC, Boyer M (1987) Diffuse noxious inhibitory controls (DNICs): psychophysical evidence in man for intersegmental suppression of noxious heat perception by cold pressor pain. Pain 30:221–232CrossRefPubMed

Tillman DB, Treede RD, Meyer RA, Campbell JN (1995) Response of C fibre nociceptors in the anaesthetized monkey to heat stimuli: estimates of receptor depth and threshold. J Physiol 485:753–765PubMed

Towell AD, Purves AM, Boyd SG (1996) CO2 laser activation of nociceptive and non-nociceptive thermal afferents from hairy and glabrous skin. Pain 66:79–86CrossRefPubMed

Tran TD, Inui K, Hoshiyama M, Lam K, Qiu Y, Kakigi R (2002) Cerebral activation by the signals ascending through unmyelinated C-fibers in humans: a magnetoencephalographic study. Neuroscience 113:375–386CrossRefPubMed

Treede RD, Meyer RA, Raja SN, Campbell JN (1992) Peripheral and central mechanisms of cutaneous hyperalgesia. Prog Neurobiol 38:397–421CrossRefPubMed

Valeriani M, Restuccia D, Le Pera D, De Armas L, Maiese T, Tonali P (2002) Attention-related modifications of ultra-late CO(2) laser evoked potentials to human trigeminal nerve stimulation. Neurosci Lett 329:329–333

Valeriani M, Arendt-Nielsen L, Le Pera D, Restuccia D, Rosso T, De Armas L, Maiese T, Fiaschi A, Tonali P, Tinazzi M (2003a) Short-term plastic changes of the human nociceptive system following acute pain induced by capsaicin. Clin Neurophysiol 114:1879–1890CrossRefPubMed

Valeriani M, de Tommaso M, Restuccia D, Le Pera D, Guido M, Iannetti GD, Libro G, Truini A, Di Trapani G, Puca F, Tonali P, Cruccu G (2003b) Reduced habituation to experimental pain in migraine patients: a CO₂ laser evoked potential study. Pain 105:57–64CrossRefPubMed

Villanueva L, Cadden SW, Le Bars D (1984) Diffuse noxious inhibitory controls (DNIC): evidence for post-synaptic inhibition of trigeminal nucleus caudalis convergent neurones. Brain Res 321:165–168CrossRefPubMed

Watanabe S, Kakigi R, Hoshiyama M, Kitamura Y, Koyama S, Shimojo M (1996) Effects of noxious cooling of the skin on pain perception in man. J Neurol Sci 135:68–73CrossRefPubMed

Title: Inhibitory effect of capsaicin evoked trigeminal pain on warmth sensation and warmth evoked potentials
Authors: Massimiliano Valeriani
Michele Tinazzi
Domenica Le Pera
Domenico Restuccia
Liala De Armas
Toni Maiese
Pietro Tonali
Lars Arendt-Nielsen
Publication date: 01-01-2005
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 1/2005
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-004-1983-1

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Inhibitory effect of capsaicin evoked trigeminal pain on warmth sensation and warmth evoked potentials

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